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Karlodinium elegans sp. nov. (Gymnodiniales, Dinophyceae), a novel species isolated from the East China Sea in a dinoflagellate bloom

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Abstract

On May 24–29, 2019, a harmful algal bloom occurred in Pingtan coastal areas, Fujian, southeast China, and caused mass mortality of cage-cultured fish. Two clonal cultures of an unknown naked dinoflagellate were set up from seawater samples taken during the bloom. The cultures were examined for morphological features, ultrastructure characters, photosynthetic pigments, the large subunit (LSU) of the rRNA gene, and the internal transcribed spacer (ITS) sequences, as well as acute toxicity analysis. The cell was unarmored, small-sized, and ovoid, and was characterized by elaborate striations on the epicone and hypocone. The nucleus was large, ellipsoid to oval or kidney-shaped, and centrally located in the cell. A long linear apical groove originated above the sulcus in the ventral epicone and extended to the dorsal side. An elongate, slit-like “ventral pore” was located on the left of the epicone, well away from the apical groove. The chloroplasts were yellowish brown, numerous, band like, and irregularly distributed in the cell periphery. Fucoxanthin was the main accessory pigment composition. Phylogeny topology reconstructed on partial LSU rDNA showed that the unknown dinoflagellate branched as a sister species to Karlodinium sp. (strain IFR981 & IFR797, from France) and Karlodinium corrugatum (strain KDGSO08, from Australia), with genetic divergences of 0.6% and 3.3%, respectively. Based on the morphological and molecular phylogenetic analysis, we describe the novel dinoflagellate as Karlodinium elegans sp. nov. A toxicity assay revealed that the clonal culture of K. elegans (strain PTB601) had no adverse effect on brine shrimp (Artemia salina) and marine medaka (Oryzias melastigma), indicating it may not be a toxic species.

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References

  • Adolf J E, Bachvaroff T R, Deeds J R, Place A R. 2015. Ichthyotoxic Karlodinium veneficum (Ballantine) J Larsen in the Upper Swan River Estuary (Western Australia): ecological conditions leading to a fish kill. Harmful Algae, 48: 83–93.

    Article  Google Scholar 

  • Bachvaroff T R, Adolf J E, Place A R. 2009. Strain variation in Karlodinium veneficum (Dinophyceae): toxin profiles, pigments, and growth characteristics. Journal of Phycology, 45(1): 137–153.

    Article  Google Scholar 

  • Bachvaroff T R, Adolf J E, Squier A H, Harvey H R, Place A R. 2008. Characterization and quantification of karlotoxins by liquid chromatography-mass spectrometry. Harmful Algae, 7(4): 473–484.

    Article  Google Scholar 

  • Benico G, Takahashi K, Lum W M, Yñiguez A T, Iwataki M. 2020. The harmful unarmored dinoflagellate Karlodinium in Japan and Philippines, with reference to ultrastructure and micropredation of Karlodinium azanzae sp. nov. (Kareniaceae, Dinophyceae). Journal of Phycology, https://doi.org/10.1111/jpy.13030.

  • Bergholtz T, Daugbjerg N, Moestrup Ø, Fernández-Tejedor M. 2006. On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. Journal of Phycology, 42(1): 170–193.

    Article  Google Scholar 

  • Cen J Y, Wang J Y, Huang L F, Ding G M, Qi Y Z, Cao R B, Cui L, Lü S H. 2020. Who is the “murderer” of the bloom in coastal waters of Fujian, China, in 2019? Journal of Oceanology and Limnology, 38(3): 722–732, https://doi.org/10.1007/s00343-019-9178-6.

    Article  Google Scholar 

  • Chakraborty S, Ramesh A, Dutta P S. 2016. Toxic phytoplankton as a keystone species in aquatic ecosystems: stable coexistence to biodiversity. Oikos, 125(5): 735–746.

    Article  Google Scholar 

  • Daugbjerg N, Hansen G, Larsen J, Moestrup Ø. 2000, Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia, 39(4): 302–317.

    Article  Google Scholar 

  • de Salas M F, Bolch C J S, Hallegraeff G M. 2005. Karlodinium australe sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic unarmoured dinoflagellate from lagoonal habitats of south-eastern Australia. Phycologia, 44(6): 640–650.

    Article  Google Scholar 

  • de Salas M F, Laza-Martínez A, Hallegraeff G M. 2008. Novel unarmored dinoflagellates from the toxigenic family Kareniaceae (Gymnodiniales): five new species of Karlodinium and one new Takayama from the Australian sector of the southern Ocean. Journal of Phycology, 44(1): 241–257.

    Article  Google Scholar 

  • Deeds J R, Terlizzi D E, Adolf J E, Stoecker D K, Place A R. 2002. Toxic activity from cultures of Karlodinium micrum (=Gyrodinium galatheanum) (Dinophyceae)—a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae, 1(2): 169–189.

    Article  Google Scholar 

  • Garcés E, Fernandez M, Penna A, Van Lenning K, Gutierrez A, Camp J, Zapata M. 2006. Characterization of NW Mediterranean Karlodinium spp. (Dinophyceae) strains using morphological, molecular, chemical, and physiological methodologies. Journal of Phycology, 42(5): 1 096–1 112.

    Article  Google Scholar 

  • Guiry M D, Guiry G M. 2020. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed on 2020-02-25.

    Google Scholar 

  • Jeffrey S W, Wright S W, Zapata M. 2011. Microalgal classes and their signature pigments. In: Roy S, Llewellyn C A, Egeland E S, Johnson G eds. Phytoplankton Pigments: Characterization, Chemotaxonomy and Applications in Oceanography. Cambridge University Press, Cambridge, United Kingdom. p.3–76.

    Chapter  Google Scholar 

  • Laza-Martinez A, Seoane S, Zapata M, Orive E. 2007. Phytoplankton pigment patterns in a temperate estuary: from unialgal cultures to natural assemblages. Journal of Plankton Research, 29(11): 913–929.

    Article  Google Scholar 

  • Li Z, Shin H H. 2018. Morphology and phylogeny of an unarmored dinoflagellate, Karlodinium jejuense sp. nov. (Gymnodiniales), isolated from the northern East China Sea. Phycological Research, 66(4): 318–328.

    Article  Google Scholar 

  • Lim H C, Leaw C P, Tan T H, Kon N F, Yek L H, Hii K S, Teng S T, Razali R M, Usup G, Iwataki M, Lim P T. 2014. A bloom of Karlodinium australe (Gymnodiniales, Dinophyceae) associated with mass mortality of cage-cultured fishes in West Johor Strait, Malaysia. Harmful Algae, 40: 51–62.

    Article  Google Scholar 

  • Litaker R W, Vandersea M W, Kibler S R, Reece K S, Stokes N A, Lutzoni F M, Yonish B A, West M A, Black M N D, Tester P A. 2007. Recognizing dinoflagellate species using ITS rDNA sequences. Journal of Phycology, 43(2): 344–355.

    Article  Google Scholar 

  • Luo Z H, Wang L, Chan L, Lu S H, Gu H F. 2018. Karlodinium zhouanum, a new dinoflagellate species from China, and molecular phylogeny of Karenia digitata and Karenia longicanalis (Gymnodiniales, Dinophyceae). Phycologia, 57(4): 401–412.

    Article  Google Scholar 

  • Nézan E, Siano R, Boulben S, Boulben S, Six C, Bilien G, Chèze K, Duval A, Le Panse S, Quéré J, Chomérat N. 2014. Genetic diversity of the harmful family Kareniaceae (Gymnodiniales, Dinophyceae) in France, with the description of Karlodinium gentienii sp. nov.: a new potentially toxic dinoflagellate. Harmful Algae, 40: 75–91.

    Article  Google Scholar 

  • Nunn G B, Theisen B F, Christensen B, Arctander P. 1996. Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. Journal of Molecular Evolution, 42(2): 211–223.

    Article  Google Scholar 

  • Pin L C, Tee L P, Ahmad A, Usup G. 2001. Genetic diversity of Ostreopsis ovata (dinophyceae) from Malaysia. Marine Biotechnology, 3(3): 246–255.

    Article  Google Scholar 

  • Rasmussen S A, Binzer S B, Hoeck C, Meier S, de Medeiros L S, Andersen N G, Place A, Nielsen K F, Hansen P J, Larsen T O. 2017. Karmitoxin: an amine-containing polyhydroxy-polyene toxin from the marine dinoflagellate Karlodinium armiger. Journal of Natural Products, 80(5): 1 287–1 293.

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12): 1 572–1 574.

    Article  Google Scholar 

  • Scholin C A, Herzog M, Sogin M, Anderson D A. 1994. Identification of group-and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. Journal of Phycology, 30(6): 999–1 011.

    Article  Google Scholar 

  • Siano R, Kooistrav, W H C F, Montresor M, Zingone A. 2009. Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia, 48(1): 44–65.

    Article  Google Scholar 

  • Tammilehto A, Nielsen T G, Krock B, Møller E F, Lundholm N. 2015. Induction of domoic acid production in the toxic diatom Pseudo-nitzschia seriata by calanoid copepods. Aquatic Toxicology, 159: 52–61.

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12): 2 725–2 729.

    Article  Google Scholar 

  • Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24): 4 876–4 882.

    Article  Google Scholar 

  • Van Wagoner R M, Deeds J R, Satake M, Ribeiro A A, Place A R, Wright J L C. 2008. Isolation and characterization of karlotoxin 1, a new amphipathic toxin from Karlodinium veneficum. Tetrahedron Letters, 49(45): 6 457–6 461.

    Article  Google Scholar 

  • Wang H X, Lu D D, Huang H Y, Göbel J, Dai X F, Xia P. 2011. First observation of Karlodinium veneficum from the East China Sea and the coastal waters of Germany. Acta Oceanologica Sinica, 32(6): 112–121.

    Article  Google Scholar 

  • Wang J Y, Cen J Y, Li S, Lü S H, Moestrup Ø, Chan K K, Jiang T, Lei X D. 2018. A re-investigation of the bloom-forming unarmored dinoflagellate Karenia longicanalis (syn). Karenia umbella) from Chinese coastal waters. Journal of Oceanology and Limnology, 36(6): 2 202–2 215.

    Article  Google Scholar 

  • Yang H J, Hu Z X, Xu N, Tang Y Z. 2019. A comparative study on the allelopathy and toxicity of four strains of Karlodinium veneficum with different culturing histories. Journal of Plankton Research, 41(1): 17–29.

    Article  Google Scholar 

  • Zapata M, Fraga S, Rodríguez F, Garrido J L. 2012. Pigment-based chloroplast types in dinoflagellates. Marine Ecology Progress Series, 465: 33–52.

    Article  Google Scholar 

  • Zapata M, Rodríguez F, Garrido J L. 2000. Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Marine Ecology Progress Series, 195: 29–45.

    Article  Google Scholar 

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Acknowledgment

Special appreciations are expressed to Prof. Moestrup of the University of Copenhagen for his helpful comments and for improving the English text. We sincerely thank Dr. JIANG Tao of the Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences for his help in the pigment composition analysis. We deeply thank Prof. Hallegraeff of University of Tasmania for his kind help on the new species confirmation.

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Authors and Affiliations

  1. Research Center of Harmful Algae and Marine Biology, Jinan University, Guangzhou, 510632, China

    Jingyi Cen, Lifen Huang, Yarou Lin, Yuzao Qi & Songhui Lü

  2. Southern Marine Science and Engineering Guangdong Laboratory, Zhuhai, 519000, China

    Songhui Lü

  3. Department of Science Research, Beijing Museum of Natural History, Beijing, 100050, China

    Jianyan Wang

  4. Fujian Fishery Resources Monitoring Center, Fuzhou, 350003, China

    Guangmao Ding

  5. Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou, 510632, China

    Jingyi Cen, Lifen Huang, Yarou Lin, Yuzao Qi & Songhui Lü

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  1. Jingyi Cen
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Correspondence to Jianyan Wang or Songhui Lü.

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Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon request.

Supported by the National Key R&D Program of China (No. 2017YFC1404301), the National Natural Science Foundation of China (Nos. 41906112, 41606175), the Science & Technology Basic Resources Investigation Program of China (No. 2018FY100200), and the Beijing Natural Science Foundation (No. 8194059)

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Cen, J., Wang, J., Huang, L. et al. Karlodinium elegans sp. nov. (Gymnodiniales, Dinophyceae), a novel species isolated from the East China Sea in a dinoflagellate bloom. J. Ocean. Limnol. 39, 242–258 (2021). https://doi.org/10.1007/s00343-020-0221-4

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